Knowledge About Emerging Zoonotic Vector-Borne Parasites Dirofilaria immitis and Dirofilaria repens in Finland: Questionnaire Survey to Medical Doctors and Veterinarians

Abstract

Zoonotic vector-borne parasites Dirofilaria immitis and Dirofilaria repens have been spreading northwards in Europe. Awareness across sectors is a key factor for preparedness to zoonotic emerging diseases. In this study, an online questionnaire was used to survey the knowledge of medical doctors and veterinarians in Finland on whether D. immitis and D. repens can infect humans and dogs, and whether these infections have been detected in Finland. Participants were recruited via two social media discussion groups, and participation was voluntary. The questionnaire was completed by 198 medical doctors and 61 veterinarians in January 2019. Knowing that D. immitis can infect both humans and dogs was indicated by the answers of 7.1% of the medical doctors and 42.6% of the veterinarians—7.6% of the medical doctors and 42.6% of the veterinarians knew D. immitis can infect humans, 9.6% of the medical doctors and 98.4% of the veterinarians knew it can infect dogs. Knowing that D. repens can infect both humans and dogs was indicated by the answers of 3.0% of the medical doctors and 60.7% of the veterinarians—3.0% of the medical doctors and 60.7% of the veterinarians knew D. repens can infect humans; 8.1% of the medical doctors and 88.5% of the veterinarians knew it can infect dogs. Overall, 4.5% of the medical doctors and 59.0% of the veterinarians selected five or more correct “yes” answers. While the results of this survey should be interpreted with caution due to limited number of participants and participation bias, they not only suggest room for improvement but also show presence of cross-sectoral knowledge. Answering “I do not know” was common. Increasing awareness about these emerging zoonotic vector-borne parasites is needed across the sectors.

Introduction

In Europe and Russia, the zoonotic vector-borne parasites Dirofilaria immitis and Dirofilaria repens have been spreading northwards (Genchi et al. 2011, Ermakova et al. 2014, Capelli et al. 2018). Finland is a Nordic country, bordering Russia, located in a region where this expansion is currently happening. Imported and travel-related Dirofilaria spp. infections have been seen in Finland and other Nordic countries (e.g., EVIRA 2014, Sævik et al. 2014, Klintebjerg et al. 2015, Vatne 2015, Saari et al. 2016, Pietikäinen et al. 2017, Tiškina et al. 2017). Recently, autochthonous infections have also been reported in the region, for example, canine infections in Estonia (Jokelainen et al. 2016), and a human case in Finland (Pietikäinen et al. 2017). The lifecycle of D. repens is well established in Russia, where the incidence of autochthonous human infections has increased (Ermakova et al. 2014, 2017, Moskvina and Ermolenko 2018).

Literature searches found no descriptions of D. immitis infections in humans from Finland, but one likely autochthonous human case of D. repens infection has been described (Pietikäinen et al. 2017). Literature searches found no descriptions of autochthonous D. immitis and D. repens infections in dogs from Finland, but imported and travel-related infections have been seen in the country (EVIRA 2014, Saari et al. 2016, Pietikäinen et al. 2017, Tiškina et al. 2017).

Transdisciplinar thinking and awareness across sectors are needed for better preparedness for emerging zoonotic parasitic vector-borne diseases (Alonso Aguirre et al., 2019). Literature searches found no publications investigating awareness or knowledge of the two parasites among medical doctors in the Nordic-Baltic region. Of veterinarians who worked in the region and who participated in a questionnaire study in 2016, 26% reportedly knew that D. immitis is zoonotic and 34% reportedly knew that D. repens is zoonotic (Tiškina et al. 2017). These results indicated a need to improve knowledge about these two emerging parasites among veterinarians in the region.

Due to the zoonotic nature of D. immitis and D. repens, there is need for awareness and knowledge about them among both medical doctors and veterinarians in countries, such as Finland, where they are imported to, spreading, and establishing. In this study, we surveyed the knowledge about D. immitis and D. repens among medical doctors and veterinarians authorized to work in Finland.

Materials and Methods

Ethical considerations

Participation was voluntary and anonymous, and the participants gave consent for their answers to be included in the study by submitting them. No personal information was collected, and the results are reported so that individual participants cannot be identified.

Setting

Finland is a Nordic country, located in northern Europe. There are ∼21,000 medical doctors and 2800 veterinarians authorized to work in the country (Finnish Medical Association 2019, Finnish Veterinary Association 2019).

Questionnaire

An online questionnaire was designed in Google Forms. The questionnaire was pretested by a group of five individuals and edited for clarity following the comments received. The questionnaire was in Finnish language. The period for answering was from January 1, 2019, to January 31, 2019. The target groups of the questionnaire were medical doctors and veterinarians who were authorized to work in Finland.

Participants were recruited via two closed social media (Facebook) discussion groups, one of medical doctors and one of veterinarians. There were 9685 and 1767 members in these groups, respectively, on March 29, 2019. The invitation messages mentioned both parasites and both target groups, as well as an encouragement to forward the link to the questionnaire to colleagues not reached by the social media group. The invitations to participate were posted on January 1, 2019, and reminders were posted on January 15, 2019.

At the beginning of the questionnaire, the aim and target group of the study were described, and it was clarified that participation was voluntary. The text explicitly advised participants to answer based on their current knowledge, without using any external information sources.

The first question in the questionnaire required an answer, other questions were voluntary. The required question asked whether the respondent was medical doctor authorized in Finland, veterinarian authorized in Finland, or neither. Those reporting themselves as either medical doctors or veterinarians were included in the study as participants, and forwarded to the three pages with the questions.

All questions were asked for D. immitis and D. repens separately. First, the participants were asked whether the parasites can infect humans and whether the parasites can infect domestic dogs. Second, the participants were asked whether any locally acquired human infections and whether any locally acquired canine infections had been detected in Finland. Third, the participants were asked whether any human infections linked to immigration or travel and whether any canine infections linked to import or travel had been detected in Finland. All questions had three answer options: “yes”, “no”, and “I do not know”.

Available literature allowed to conclude that the correct answer was “yes” for seven of the questions (EVIRA 2014, Saari et al. 2016, Pietikäinen et al. 2017), and we considered selecting five or more correct “yes” answers as an indication of high level of knowledge.

Statistical analyses

Data were handled in Excel and analyzed using OpenEpi (Dean et al. 2017) and Stata 13.1 (StataCorp, College Station, TX). In addition to descriptive statistics, we compared the answers of medical doctors versus veterinarians. Not answering was treated as missing data. We calculated 95% confidence intervals (CIs) for the proportions (Mid-p Exact, OpenEpi) and for odds ratios (as reported by Stata). For comparing proportions, we used two-by-two tables and calculated 2-tailed p values (Mid-p Exact).

Results

Of the 260 respondents, one was self-reportedly neither a medical doctor nor a veterinarian. The final sample size was thus 259 participants, comprising 198 medical doctors (76.4%) and 61 veterinarians (23.6%). The participation percentage was <3.5% of the individuals the social media groups could reach and <2.5% of the whole professions (Finnish Medical Association 2019, Finnish Veterinary Association 2019). One medical doctor left all questions unanswered but was considered as having completed the questionnaire, as the empty answers were submitted. Other missing data were single questions left unanswered by four participants, who were all medical doctors.

Table 1 shows the number and proportion of participants who selected each of the options for the questions, by whether they were medical doctors or veterinarians. Overall, the option “I do not know” was commonly selected.

Table 1.

Number and Proportion of Participants Who Selected Each of the Options for the Questions Surveying Knowledge About Dirofilaria immitis and Dirofilaria repens in Finland, January 2019

Questions	Answer options^a	Medical doctors (n = 198), n (%)	Veterinarians (n = 61), n (%)	p value ^b
Can D. immitis infect humans?	Yes	15 (7.6)	26 (42.6)	<0.001
	No	4 (2.0)	11 (18.0)
	I do not know	178 (89.9)	24 (39.3)
	No reply	1 (0.5)	0 (0.0)
Can D. immitis infect domestic dogs?	Yes	19 (9.6)	60 (98.4)	<0.001
	No	0 (0.0)	0 (0.0)
	I do not know	177 (89.4)	1 (1.6)
	No reply	2 (1.0)	0 (0.0)
Can D. repens infect humans?	Yes	6 (3.0)	37 (60.7)	<0.001
	No	6 (3.0)	3 (4.9)
	I do not know	184 (92.9)	21 (34.4)
	No reply	2 (1.0)	0 (0.0)
Can D. repens infect domestic dogs?	Yes	16 (8.1)	54 (88.5)	<0.001
	No	0 (0.0)	0 (0.0)
	I do not know	180 (90.9)	7 (11.5)
	No reply	2 (1.0)	0 (0.0)
Have there been any locally acquired human D. immitis infections in Finland?	Yes	3 (1.5)	1 (1.6)
	No	11 (5.6)	20 (32.8)
	I do not know	183 (92.4)	40 (65.6)
	No reply	1 (0.5)	0 (0.0)
Have there been any immigration- or travel-related human D. immitis infections in Finland?	Yes	4 (2.0)	16 (26.2)
	No	6 (3.0)	2 (3.3)
	I do not know	187 (94.4)	43 (70.5)
	No reply	1 (0.5)	0 (0.0)
Have there been any locally acquired canine D. immitis infections in Finland?	Yes	2 (1.0)	6 (9.8)
	No	13 (6.6)	38 (62.3)
	I do not know	182 (91.9)	17 (27.9)
	No reply	1 (0.5)	0 (0.0)
Have there been any import- or travel-related canine D. immitis infections in Finland?	Yes	15 (7.6)	53 (86.9)	<0.001
	No	2 (1.0)	0 (0.0)
	I do not know	180 (90.9)	8 (13.1)
	No reply	1 (0.5)	0 (0.0)
Have there been any locally acquired human D. repens infections in Finland?	Yes	3 (1.5)	6 (9.8)	0.007
	No	10 (5.1)	12 (19.7)
	I do not know	184 (92.9)	43 (70.5)
	No reply	1 (0.5)	0 (0.0)
Have there been any immigration- or travel-related human D. repens infections in Finland?	Yes	3 (1.5)	20 (32.8)
	No	7 (3.5)	0 (0.0)
	I do not know	187 (94.4)	41 (67.2)
	No reply	1 (0.5)	0 (0.0)
Have there been any locally acquired canine D. repens infections in Finland?	Yes	3 (1.5)	6 (9.8)
	No	9 (4.6)	28 (45.9)
	I do not know	185 (93.4)	27 (44.3)
	No reply	1 (0.5)	0 (0.0)
Have there been any import- or travel-related canine D. repens infections in Finland?	Yes	13 (6.6)	47 (77.0)	<0.001
	No	0 (0.0)	0 (0.0)
	I do not know	183 (92.4)	14 (23.0)
	No reply	2 (1.0)	0 (0.0)

The options considered correct (supported by available literature) are highlighted with bold.

The proportion of the medical doctors versus the proportion of the veterinarians selecting the correct answer (p value, Mid-p Exact).

Knowing that D. immitis can infect both humans and dogs was indicated by the answers of 14 (7.1%; 95% CI: 4.1–11.3) of the medical doctors and 26 (42.6%; 95% CI: 30.7–55.2) of the veterinarians (p value <0.001). Knowing that D. repens can infect both humans and dogs was indicated by the answers of 6 (3.0%; 95% CI: 1.2–6.2) of the medical doctors and 37 (60.7%; 95% CI: 48.0–72.3) of the veterinarians (p value <0.001).

High level of knowledge, selecting five or more correct “yes” answers, was reached by 9 (4.5%; 95% CI: 2.2–8.2) of the medical doctors and 36 (59.0%; 95% CI: 46.4–70.8) of the veterinarians (p value <0.001). Veterinarians had 30 times higher odds (95% CI: 13.0–70.1) to have selected five or more correct answers than medical doctors did.

Discussion

We surveyed knowledge on two emerging zoonotic vector-borne parasites, D. immitis and D. repens, in both medical doctors and veterinarians in Finland, a country where these two parasites have been described in imported or traveled dogs (EVIRA 2014, Saari et al. 2016, Pietikäinen et al. 2017, Tiškina et al. 2017) and where the first autochthonous human D. repens infection has been diagnosed a few years ago (Pietikäinen et al. 2017). While the results indicate room for improvement in knowledge about these parasites, presence of knowledge across sectors was also evident.

Despite their limitations, questionnaire surveys may serve to investigate the spread of newly emerged pathogens, to increase awareness, and to help in planning continuing professional education and further studies (e.g., Tiškina et al. 2017, 2019). Our survey was answered by a sufficient number of participants to obtain an overview and make comparisons. However, the number of participants was limited, and participation bias is important to emphasize; the participants of our survey may not represent the two professions well. The recruiting did not reach all medical doctors and veterinarians, the questionnaire was open for answers for a limited time period, the questionnaire was available only in Finnish, and participation was voluntary. For example, individuals who were interested in parasites, who were active in social media, or who had a positive attitude toward questionnaire studies were perhaps overrepresented. However, participation bias was expected to be similar in both groups.

Another challenge of questionnaire-derived data is lack of confirmation. Because closed discussion groups were used for recruiting and the target groups were indicated at the beginning of the questionnaire, the participants likely comprised only medical doctors and veterinarians authorized in Finland, despite this was not confirmed by the authors.

The participants were instructed to answer without using external information sources, but whether this was followed could not be confirmed. Many participants selected “I do not know” to several of the questions, which perhaps supports this advice being followed. Providing this option ensured that the participants were not forced to guess between “yes” and “no”. It should be emphasized that in a normal situation, the medical doctors and veterinarians have possibilities to consult literature and colleagues. The results of this survey encourage cross-sectoral consultations.

Both D. immitis and D. repens are zoonotic, and presence of infected dogs implies risk of human infections (Simón et al. 2012). Both medical doctors and veterinarians are needed to address zoonotic challenges (Alonso Aguirre et al., 2019). In this study, veterinarians appeared to have better knowledge about the two parasites than medical doctors did. This may be due to the fact that these parasites are primarily canine parasites. There has also been continuing professional education on this topic for veterinarians in the last years, as well as published factsheets (FECAVA 2018).

Perhaps some of the awareness among veterinarians is also due to the previous questionnaire survey (Tiškina et al. 2017) that was targeted to veterinarians and used the same social media group as one of the ways to recruit participants. The results from this survey and that previous survey are not directly comparable, but the proportion indicating knowing about zoonotic nature of these parasites seems to have increased. In 2016, 26% of veterinarians working in the Nordic-Baltic region reportedly knew that D. immitis is zoonotic and 34% reportedly knew that D. repens is zoonotic (Tiškina et al. 2017) versus in this study, 42.6% of participating veterinarians authorized to work in Finland answered that D. immitis can infect both humans and dogs, and 60.7% answered that D. repens can infect both humans and dogs.

Moreover, zoonotic potential of pathogens and One Health thinking have perhaps been more emphasized in the veterinary profession than in the human medical profession. For example, the national legislation mentions preserving public health among the objectives of the professional activity of the veterinary profession (Ministry of Agriculture and Forestry 2000).

While up-to-date knowledge is important, misconceptions may be particularly harmful. Almost one fifth of the veterinarians erroneously claimed that D. immitis would not be able to infect humans (Table 1). This parasite has been seen in Finland in imported dogs (Saari et al. 2016, Tiškina et al. 2017), and while it is an important pathogen for the dogs themselves, it should also be remembered as a zoonotic parasite of public health relevance. Five percent of medical doctors erroneously answered that there would not have been any autochthonous human D. repens case in Finland, while only 1.5% indicated correctly knowing that there is (Table 1). Awareness is low, despite the case was published in an open access journal (Pietikäinen et al. 2017). Publishing new findings is a prerequisite for increasing knowledge and awareness and should be encouraged. Moreover, wide availability and efficient dissemination of published, new information merits more attention.

The authors of this study might also have knowledge gaps—for example, some participants answered that there would have been locally acquired D. immitis infections in Finland (Table 1), but extensive literature searches found no reports thereof, and thus the question could not be included in the evaluation of level of knowledge.

It needs to be emphasized that both professions targeted in this study encompass a wide variety of work types. For some, these parasites are of little direct relevance, and the need to know about them can be questioned. However, these parasites can be encountered in a wide variety of types of work, and in general, One Health preparedness, including awareness of new trends in the field of zoonotic diseases, is of importance in both professions.

Practicing medical doctors and veterinarians should be aware of these parasites, for example, as possible differential diagnoses for tumors and unspecific clinical signs. One of the reasons why the canine infections need to be prevented efficiently and diagnosed and treated early by veterinarians is that these parasites are zoonotic. To be able to manage the risk of human infections, it is important that medical doctors know that dogs are the key hosts that provide the microfilariae to mosquitoes, if infected and not treated. Monitoring the evolving situation and discussing possible control measures across the sectors would be welcomed, preferably in international collaboration across the region where the topic is extremely timely.

Footnotes

Acknowledgments

We warmly thank all the participants.

Author Disclosure Statement

P.J. has received lecture fees from Sympaatti, Evidensia/Vetcare, Orion Pharma Eläinlääkkeet, and Fennovet. The other authors declare no conflicts if interest.

References

Alonso Aguirre

, Basu

, Kahn

, Morin

, et al. Transdisciplinary and social-ecological health frameworks—Novel approaches to emerging parasitic and vector-borne diseases. Parasite Epidemiol Control, 2019; 4:e00084.

Capelli

, Genchi

, Baneth

, Bourdeau

, et al. Recent advances on Dirofilaria repens in dogs and humans in Europe. Parasit Vectors, 2018; 11:663.

Dean

, Sullivan

, Soe

. OpenEpi: Open source epidemiologic statistics for public health, version 3.01. 2017. Available at www.openepi.com/ (accessed April 25, 2019 ).

Ermakova

, Nagorny

, Pshenichnaya

, Ambalov

, et al. Clinical and laboratory features of human dirofilariasis in Russia. IDCases, 2017; 9:112–115.

Ermakova

, Nagorny

, Krivorotova

, Pshenichnaya

, et al. Dirofilaria repens in the Russian Federation: Current epidemiology, diagnosis, and treatment from a federal reference center perspective. Int J Infect Dis, 2014; 23:47–52.

EVIRA (currently: Finnish Food Authority). Uusi loistartunta Suomeen tuodussa koirassa [New parasitic infection in a dog imported to Finland.]. 2014. https://www.ruokavirasto.fi/viljelijat/elaintenpito/elainten-terveys-ja-elaintaudit/elaintaudit/lemmikkielaimet/koirat/koirien-maahantuontiin-liittyvat-riskit/dirofilaria-repens/ (accessed April 25, 2019 ).

FECAVA, in collaboration with ESCCAP and ESDA. Factsheets. 2018. Available at https://www.fecava.org/en/policies-actions/factsheets (accessed April 25, 2019 ).

Finnish Medical Association. 2019. Available at https://www.laakariliitto.fi/en/ (accessed April 25, 2019 ).

Finnish Veterinary Association. 2019. Available at https://www.sell.fi/elainlaakarin-ammatti (accessed April 25, 2019 ).

10.

Genchi

, Kramer

, Rivasi

. Dirofilarial infections in Europe. Vector Borne Zoonotic Dis, 2011; 11:1307–1317.

11.

Jokelainen

, Mõtsküla

, Heikkinen

, Ülevaino

, et al. Dirofilaria repens microfilaremia in three dogs in Estonia. Vector Borne Zoonotic Dis, 2016; 16:136–138.

12.

Klintebjerg

, Petersen

, Pshenichnaya

, Ermakova

, et al. Periorbital Dirofilaria repens imported to Denmark: A human case report. IDCases, 2015; 2:25–26.

13.

Ministry of Agriculture and Forestry, Finland. Act on access to and pursuit of the profession of veterinary surgeon. 2000. Available at https://www.finlex.fi/en/laki/kaannokset/2000/en20000029_20101087.pdf (accessed April 25, 2019 ).

14.

Moskvina

, Ermolenko

. Dirofilariasis in Russian Federation: A big problem with large distribution. Russ Open Med J, 2018; 7:1.

15.

Pietikäinen

, Nordling

, Jokiranta

, Saari

, et al. Dirofilaria repens transmission in southeastern Finland. Parasit Vectors, 2017; 10:561.

16.

Saari

, Näreaho

, Nikander

. Elinympäristönä Koira—Koiran Loiset ja Loissairaudet [Dog as living environment – parasites and parasitic diseases of dogs] [In Finnish] . Helsinki: Fennovet Oy, Grano Oy, 2016: 244.

17.

Sævik

, Jörundsson

, Stachurska-Hagen

, Tysnes

, et al. Dirofilaria repens infection in a dog imported to Norway. Acta Vet Scand, 2014; 56:6.

18.

Simón

, Siles-Lucas

, Morchón

, Gonzláez-Miguel

, et al. Human and animal dirofilariasis: The emergence of a zoonotic mosaic. Clin Microbiol Rev, 2012; 25:507–544.

19.

Tiškina

, Jokelainen

. Vector-borne parasitic infections in dogs in the Baltic and Nordic countries: A questionnaire study to veterinarians on canine babesiosis and infections with Dirofilaria immitis and Dirofilaria repens . Vet Parasitol, 2017; 244:7–11.

20.

Tiškina

, Lindqvist

, Blomqvist

, Orav

, et al. Autochthonous Angiostrongylus vasorum in Finland. Vet Rec Open, 2019; 6:e000314.

21.

Vatne

. Heartworm infection caused by Dirofilaria immitis in a dog imported to Norway. Eur J Companion Anim Pract, 2015; 25:60–67.